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Visual Evoked Potentials in the Horse

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Visual Evoked Potentials in the Horse Visual evoked potentials in the horse Lena Ström Faculty of Veterinary Medicine and Animal Science Department of Clinical Sciences Uppsala Doctoral thesis Swedish University of Agricultural Sciences Uppsala 2019 Acta Universitatis Agriculturae Sueciae 2019:53 Cover illustration: L. Adehed ISSN 1652-6880 ISBN (print version) 978-91-7760-424-2 ISBN (electronic version) 978-91-7760-425-9 © 2019 Lena Ström, Uppsala Print: SLU Service/Repro, Uppsala 2019 Visual evoked potentials in the horse Abstract Vision is an important sense for horses, both for survival in the wild and when horses are used for work, sport or recreation. However, it is often difficult to diagnose visual impairment in this species. Traditional techniques available in clinical equine practice, are based on subjective evaluations, and their results are many times difficult to interpret. Electrodiagnostic methods, flash electroretinography (FERG) and recording of flash visual evoked potentials (FVEP) are used to objectively evaluate the function of the retinal and post-retinal visual pathways. The electrical potentials generated in response to brief visual stimuli are measured non-invasively. Abnormal function in visual pathways can affect the FERG and FVEP waveforms, peak times and amplitudes. Lesions can thereby be detected, and their approximate localization evaluated. FVEPs are used in human medicine, and occasionally in animal species, but have not been described in the horse. The general aim of this thesis was to establish a technique for recording of FVEPs in horses in clinical practice. The results showed that FVEPs can be readily recorded in sedated horses in a clinical setting. The recorded waveform consisted of a series of positive (P1-P5) and negative (N1-N2) wavelets. The overall appearance of the waveform was shown to be similar in foals, young horses and adult horses. An age-related effect on peak times and amplitudes was observed, but most of the changes occurred early in life. Important data on FVEP variability and repeatability was reported, and it was concluded that P2, N2 and P4 peak times should be included in the evaluation of equine, clinical FVEPs. The large inherent variability of FVEP amplitudes made them less useful, but they occasionally provided support to a clinical diagnosis. In clinical patients, electrodiagnostic testing helped assessing functional impact of potentially visual-threatening diseases. By recording FERGs and FVEPs simultaneously, a subdivision into retinal vs post-retinal dysfunction could be made in many patients, such as horses with optic neuropathies and cortical visual impairment. FVEPs may also be of prognostic value in horses with traumatic optic neuropathy and possibly in cases with cortical visual impairment. The results from this thesis, opens up for the use of the FVEP as an adjunctive, objective method in the evaluation of equine patients with suspected visual impairment and neurological disease, but also for studies of development and function of the visual pathways in this species. Keywords: visual evoked potential, VEP, electroretinogram, ERG, horse, vision, visual impairment, blindness, retina, optic nerve, visual cortex Author’s address: Lena Ström, SLU, Department of Clinical Sciences, P.O. Box 7054, 750 07 Uppsala, Sweden Visual evoked potentials in the horse Abstract Synen är ett viktigt sinne för hästen, både för överlevnad i det vilda och när hästar används för arbete, sport eller rekreation. Det är ofta svårt att diagnostisera synnedsättningar hos häst. De tekniker som används i klinisk verksamhet i dagsläget, baseras på subjektiv utvärdering, och resultaten från dessa undersökningar är ofta svåra att tolka. Elektrodiagnostiska metoder, elektroretinografi (flash-ERG, FERG) och visuella retningspotentialer (flash-VEP, FVEP) kan användas för att objektivt utvärdera funktionen i retina och post-retinala synbanor. De elektriska potentialer som genereras som svar på ljusblixtar registreras icke-invasivt med elektroder. Nedsatt funktion i synbanorna kan påverka latenstider och amplituder i den vågform som registreras. Lesioner kan därmed detekteras och ungefärlig lokalisation fastställas. FVEP används inom humansjukvården, och ibland även på djur, men har inte beskrivits hos djurslaget häst. Övergripande syfte med denna avhandling var att utveckla en teknik för registrering av FVEP hos häst i klinisk verksamhet. Resultaten visade att FVEP kan registreras på häst under klinikförhållanden. Vågformen bestod av en serie av positiva (P1-P5) och negativa (N1-N2) toppar och dalar. Vågformens utseende var i huvudsak lika mellan föl, unga samt vuxna hästar. En åldersrelaterad effekt observerades för latenstider och amplituder, främst under de första åren i livet. Metodens variabilitet och repeterbarhet utvärderades, och latenstiderna för P2, N2 och P4 visades vara användbara vid utvärdering av hästens FVEP. Amplituderna var mer variabla, även om de kunde bidra med kliniskt relevant information vid vissa diagnoser. Elektrodiagnostik visades ge värdefull information vid utvärdering av synnedsättning hos häst. Genom att registrera FERG och FVEP samtidigt, kunde retinal dysfunktion skiljas från post-retinala problem hos många patienter, till exempel vid traumatisk optikusneuropati och vid kortikal påverkan. Resultaten från detta arbete möjliggör för användning av FVEP som en objektiv utvärderingsmetod, tillsammans med övriga undersökningar av hästpatienter med synnedsättningar och/eller neurologisk sjukdom, samt även för användning vid studier av synbanornas normala funktion och utveckling hos detta djurslag. Keywords: visual evoked potential, VEP, elektroretinogram, ERG, häst, syn, synnedsättning, blindhet, retina, synnerv, synkortex Author’s address: Lena Ström, SLU, Department of Clinical Sciences, P.O. Box 7054, 750 07 Uppsala, Sweden To my family Peter, Gustav, Marcus, Erik och min pappa Sören “An imperfect apprehension of the sensory world of animals usually prevents our being able to speak confidently of what the ‘vision’ of a given species is like. On the other hand, familiarity with the structure and physiological reactions of its eyes, together with an understanding of its behavior and requirements can, perhaps, enable us to make not too foolish a guess.” Dr Katherine Tansley in Vision in Vertebrates, 1965 Contents List of publications 9 Abbreviations 11 1 Introduction 13 1.1 Vision 13 1.2 Vision in the horse 14 1.2.1 Ocular adaptations 14 1.2.2 Visual pathways 15 1.3 Evaluation of visual impairment in the equine patient 18 1.3.1 Neuro-ophthalmic examination 18 1.3.2 Falling cotton-ball test and obstacle course evaluation 19 1.3.3 Ophthalmic examination 20 1.4 Visual impairment in horses 20 1.5 Electrophysiology 21 1.5.1 History 21 1.5.2 Clinical use 22 1.5.3 Electrodiagnostic testing in medicine 22 1.5.4 ERGs and VEPs in animals 23 2 Aims 25 3 Materials and methods 27 3.1 Horses 27 3.2 Methods of examinations 28 3.3 Sedation and preparations 29 3.4 Electrophysiological recordings 29 3.4.1 FERGs 30 3.4.2 FVEPs 30 3.5 Evaluation of FERGs and FVEPs 32 3.6 Statistical analyses 32 3.6.1 Paper I 33 3.6.2 Paper II 33 3.6.3 Paper III 33 3.6.4 Paper IV 34 4 Results 35 4.1 The normal Equine FVEP (I) 35 4.2 Age-associated changes in the equine FVEP (II) 36 4.3 Variability, repeatability and test-retest reliability of the equine FVEP (III) 37 4.4 Electrodiagnostic findings in horses with visual impairment (IV) 38 5 General discussion 41 5.1 The normal equine FVEP waveform (I) 41 5.2 Technical aspects (I-IV) 43 5.3 Age-associated changes (II) 45 5.4 Variability and normal reference data (III) 47 5.5 Electrodiagnosic testing in the evaluation of the equine patient with visual impairment (IV) 49 6 Conclusions 55 7 Future perspectives 57 References 59 Popular science summary 67 Populärvetenskaplig sammanfattning 71 Acknowledgements 75 List of publications This thesis is based on the work contained in the following papers, referred to by Roman numerals in the text: I Ström L* & Ekesten B (2016). Visual evoked potentials in the horse. BMC Veterinary Research, 12:120. II Ström L*, Michanek M, Ekesten B (2019). Age-associated changes in the equine flash visual evoked potential. Veterinary Ophthalmology, 22 (4):388-397. III Ström L*, Bröjer J, Ekesten B. Variability, repeatability and test-retest reliability in equine flash visual evoked potentials. Submitted manuscript. IV Ström L*, Källberg M.E, Nostell K, Ekesten B. Electrophysiological assessment in horses with visual impairment. In manuscript. Papers I-II are reproduced with the permission of the publishers. * Corresponding author 9 The contribution of Lena Ström to the papers included in this thesis was as follows: I Participation in the design of the study, acquisition, analysis and interpretation of data, drafting the article, critical revision of the article. II Participation in the design of the study, acquisition, analysis and interpretation of data, drafting the article, critical revision of the article. III Participation in the design of the study, acquisition, statistical analysis and interpretation of data, drafting the article, critical revision of the article. IV Participation in the design of the study, acquisition, analysis and interpretation of data, drafting the article, critical revision of the article. 10 Abbreviations BHL: bullet-hole lesion CI: confidence interval CR: coefficient of repeatability CV: coefficient of variation ERG: electroretinogram/electroretinography FERG: flash electroretinogram/electroretinography FVEP: flash visual evoked potential
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